Morphogens in biological development: Drosophila example

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1 LSM5194 Morphogens in biological development: Drosophila example Lecture 29

2 The concept of morphogen gradients The concept of morphogens was proposed by L. Wolpert as a part of the positional information theory in Morphogen gradients can be very shallow and very sharp. In Xenopus, gradient of activin can be formed experimentally over 100 um in 1 hour. Teleman et al., Cell v 105, p 559, 2001 Tabata, Nat Rev Gen v 2, p 620, 2001 Several mechanisms have been proposed for the propagation of morphogens through the tissue: diffusion transcytosis endocytic relay from cell to cell cell-cell contact by cytonemes

3 The master plan of the Drosophila embryo The creation of the body plan of Drosophila by the gradient forming proteins is perhaps the best understood morphogenetic process. Formation of morphogenetic fields starts on the acellular level of syncytium. Unless specified otherwise, the illustrations are from Wolpert et al, Principles of development. 2002

4 Maternal genes define the body axes Both anterior-posterior and dorsal-ventral axes are defined by deposition of maternal mrna which is transcribed after fertilization. The anterior end is defined by gene bicoid while the anterior end is defined by a group of 9 genes including nanos and caudal (red image below).

5 Dorso-ventral axis uses different mechanism Specification of dorso-ventral axis occurs through activation of maternally deposited gene dorsal by means of extracellular ligand spatzle deposited on the ventral part of the egg shell through activation of Toll signaling pathway (analogue of the NF-kB pathway).

6 Zygotic genes do actual segmentation work Upon establishment of the gradient of dorsal, the rest of the dorso-ventral pattern consisting of the 6 segments is done by a group of 7 proteins that pattern ventral side (rhomboid, twist and snail) separately from dorsal (dpp, tolloid and zernknullt). The final result is achieved through a complex activation-inhibition pattern of gene expression.

7 Gap genes pattern antero-posterior axis After establishment of the antero-posterior gradient of maternal genes, the zygotic gap genes switch on. Hunchback is directly induced by bicoid while giant, kruppel and knirps are induced downstream of hunchback. All gap genes are transcription factors necessary for the following tissue patterning. The shown spatial patterns of expression result from complex pattern of mutual activation and inhibition.

8 Segmentation and pair-rule genes Shortly after the gap genes, pair-rule genes eve and fushi tarazu create 14 stripes of alternating expression which will become after some modification the segments of the larval body. Each strip has its own genetic control and is not a result of a periodic process!

9 Segment polarity genes finalize segmentation Segment polarity genes finally mark the boundaries of the body segments and provides them with antero-posterior direction. The genes of this group code for such important morphogens like wingless, engrailed and hedgehog and they are connected by complex interaction network.

10 Selector and homeotic genes define future of segments Finally, the future of the Drosophila segments is defined by homeotic and selector genes which are homologous to the Hox genes of vertebrates. These genes can change the whole organ into another organ. For example, mutation antennapedia results in substitution of antennae by legs. The relationship to simple gradients can hardly be followed on this level of development.

11 What to take home Morphogenesis in real biological systems is controlled by complex networks of morphogens Each of them forms only simple gradient, yet the combination of these simple prepatterns being superimposed on each other can define layout of any complexity The relative importance of morphogen gradients diminishes with the size of embryo and with the level of development To achieve necessary robustness and scale independence, morphogenetic networks must possess high redundancy and non-linearity achieved through multiple positive and negative feedback loops

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